A Four-year Study of the Association Between Male Dominance Rank, Residency Status, and Reproductive Activity in Rhesus Macaques (Macaca mulatta)

PRIMATES, 40(1): 159--175, January 1999 159 Special Edition: Primate Socioecology

A Four-year Study of the Association Between Male Dominance Rank, Residency Status, and Reproductive Activity in Rhesus Macaques (Macaca mulatta)

JOHN BERARD University of Puerto Rico, Medical Sciences Campus

ABSTRACT. Considerable controversy exists on the nature of the relationship between male dominance rank and reproductive activity. The nature of this relationship has important implications for understanding the manner in which males compete for access to limited resources. Behavioral data on mating patterns were collected over a four-year period from one social group of rhesus macaques on Cayo Santiago. Correlations between dominance rank and reproductive activity were not stable over a four-year period, but changed yearly. Positive, significant correlations were present in the first two years of the study while non-significant correlations were found in the second two years. The variation found in the correlations between rank and mating activity could be accounted for by changes in the mating frequencies of different classes of males. The long-term resident males had declines in ejaculation frequencies over the duration of the study. Males who immigrated into the group had yearly increases in reproductive behavior over three consecutive years. Maturing natal males also increased their levels of reproductive activity from year-to- year. Combining these mating patterns over time resulted in shifting the proportions of matings away from the long-term residents and in favor of the new males. High-ranking males had an advantage in reproductive activity over the first two years of the study, as measured by both the total number of ejaculations and the mean number of ejaculation per male. New males, comprised of recent immigrants and maturing natal males, had a greater level of reproductive activity over the last two years. These results suggest that the effect of rank on reproductive activity is variable and that males utilize alternative tactics to attain access to limited resources. Simple one-factor models explaining the relationship between rank and reproductive activity must be replaced with models explaining how alternate strategies affect male competition and reproductive success in primates.

Key Words: Dominance rank; Reproductive behavior; Mating success; Immigration; Cayo Santiago.

INTRODUCTION

The nature of the relationship between male dominance rank and reproductive activity has been investigated more thoroughly in the Order Primates than any other taxon (DEws~uRV, 1982; FEDIGAN, 1983). Despite the plethora of studies, a consensus on the degree and nature of the impact of rank on reproduction has not been reached.

For many years it was easy to comprehend, both theoretically and empirically, the relationship between male dominance rank and reproductive activity. It was postulated that certain physical (e.g. size) or behavioral (e.g. aggressive) characteristics would provide individual males with an advantage in aggressive competit ion with other males. Males would fight with the victor becoming high-ranking. High-ranking males would then have a priority of access to resources, including access to mating partners, and contribute a disproportionately large number of offspring to the next generation. Those offspring would then perpetuate those characters that contributed to high dominant status. Thus an aggressive competit ion model, a logical theory relating dominance to mating and reproduction, evolved. The implicit theoretical hypothesis

160 J. BERARD

was that the agonistic interactions determining dominance rank were a form of intrasexual competition for access to fertile females (BERENSTAIN & WADE, 1983; SMUTS, 1987).

With the firm establishment of a theoretical framework that directly tied male reproduction to dominance rank, numerous studies were conducted to collect empirical data to support this notion. A wide range of studies over a broad range of primate taxa affirmed the relationship between dominance and mating success (see COWLISHAW & DUNBAR, 1991 for review). As studies reporting a lack of a significant correlation between reproductive activity and dominance rank began to accumulate (Lou 1971; SUClYAMA, 1971; TUTIN, 1979; STRUM, 1982; SMUTS, 1985; BERCOVITCH, 1986), it became difficult to explain these irregularities within the heuristic framework provided by the aggressive competition model. Consequently, the validity of the relationship between rank and reproduction came into question (BERNSTEIN, 1976; STRUM, 1982; FED1GAN, 1983).

The development of DNA techniques to establish paternity promised to resolve the issue of the relationship between rank and reproduction by the direct test of the hypothesis that high- ranking males sire a disproportionate number of offspring. Unfortunately, results from these studies are just as equivocal as the results from behaviorally oriented studies. While some studies found that high-ranking males did sire a greater proportion of offspring than their competitors (DE RUITER et al., 1992; DE RUITER & VAN HOOFF, 1993; Dixson et al., 1993; PAUL et ai., 1993; BAUERS & HEARN, 1994) others found this was not the case (BERARD et al., 1993; INOUE et al., 1993). Instead of resolving the issue, studies utilizing paternity techniques contributed to the lack of consensus on the relationship between rank and reproduction.

The lack of consensus across the primate order is not surprising given the great diversity of primates, forms of mating and social systems, and types of habitats. Even within the genus Macaca there are considerable inter-specific differences in behavior, social organization, ecology, breeding seasonality, dominance acquisition, and breeding patterns (CALDECOTT, 1986; FA & LINDBURG, 1996) making it difficult to derive universal rules governing the effect of rank on reproductive activity.

Limiting the analysis of the effect of rank on reproductive activity to one species from one study site might serve to clarify the issues. A number of studies on reproductive behavior have been conducted on the rhesus macaques at Cayo Santiago. Some studies have demonstrated that high dominance rank corresponds with high rates of reproductive activity (CARPENTER, 1942; CONAWAY & KOFORD, 1964; KAUFMANN, 1965; CHAPAIS, 1983a; HILL, 1987; MANSON, 1992; BERARD et al., 1993) while other studies have found no such correlation (LoY, 1971; MCM1LLAN, 1989). Despite methodological problems (e.g. observability of matings by low-ranking males: DRICKAMER, 1974) and differences in behavioral measures and definitions across studies (e.g. BERNSTEIN, 1981), there remained conflicting conclusions from the same species at the same study site. How does one account for these differences if rank were so clearly tied to reproduction?

One possible explanation is that many studies have encompassed only one mating season. A variety of conclusions are possible in a single-year study because random fluctuations in behaviors, such as few immigrants or a high rate of mating by one particular individual, may have a significant effect on the outcome. A one-year study provides useful information, but tells little of the complexity or the processes involved in the relationship between rank and reproductive activity. Placing reproductive activity in the context of a male's life history (e.g. STRUM, 1994) affords the opportunity to understand the conditions and circumstances under which rank influences reproductive activity.

Various effects of length of residency on the relationship between rank and mating have been suggested. Tenure length, dominance rank, and age are interrelated and are affected by previous reproductive activity. In turn, they will affect future reproductive and mating success (STRUM,

Dominance and Reproductive Activity in Rhesus Macaques 161

1982, 1994; TAKAHATA, 1982; NOE & SLUIJTER, 1990; HUFFMAN, 1991, 1992). Factors such as the history of the social group, the tenure length of the males, the number of immigrants, and the number of maturing natal males will all influence the relationship between male dominance rank and reproductive activity (CowLISHAW & DUNBAR, 1991).

This study presents the results of the first five years of an eight-year study on mating patterns and paternity in the rhesus macaques on Cayo Santiago. Of particular interest are the circumstances surrounding change in reproductive activity and the observation that tenure length and rates of immigration alter the relationship between rank and mating. Through the use of data from a long-term study of mating patterns, it will be demonstrated that: (1) the mating success of high-ranking, long-term resident males decrease over time; and (2) the mating success of recent immigrants increases over time. Thus, within the same social group, there are yearly changes in mating frequencies by different classes of males that affect correlations between male dominance and reproductive activity.

METHODS

The study was conducted in the colony of rhesus macaques (M. mulatta) on Cayo Santiago (18~ 65~ See SADE et al. (1985) and RAWLINS and KESSLER (1986) for a complete history of the colony. Cayo Santiago is a hilly, heavily vegetated island located off the south- eastern coast of Puerto Rico. Cliffs rising to 30 m are located on the eastern and southern end of the island. The animals are provisioned once daily with 0.23 kg commercial monkey chow per monkey. In addition, the animals spend half of their feeding time foraging on the natural vegetation (MARRIOTT et al., 1989).

The data were collected over a five-year period from one social group (Group S). Only data from four years, 1988, 1990, 1991, and 1992 were used. Data from 1989 were excluded because Hurricane Hugo hit Cayo Santiago one-third of the way through the mating season making further behavioral observations impossible. The group size ranged from 54 animals in 1988 to 98 in 1992. This included from 18 to 30 females >3 yr of age and 12 to 22 group males > 4 yr of age over the five-year period. Table 1 lists the group composition of Group S during the study period.

Data were collected by a team of trained observers during all-day focal follows of estrous females. There were three observers in 1988, seven in 1990, ten in 1991, and ten in 1992. All observers were trained and passed a reliability test at the 90% level. Females 3 yr of age and older were checked daily for signs of estrous. A female was considered to be in estrous when she met one of the two following criteria: (1) if she had a sperm plug; or (2) was involved in a mount series of three or more consecutive mounts. Once it was determined which females were

Table 1. Composition of Group S and the number of ejaculations, 1988-1992. Ejaculations

Year Group size Males (-->4 yr) Females (-->3 yr) Total Conception 1988 54 13 18 106 55 1989 67 14 19 - - 1990 74 17 20 237 54 1991 88 23 25 582 147 1992 98 22 30 464 189

Total: Ejaculations for all cycles; Conception: the number of ejaculations during conception cycles only. See text for definitions.

162 J. BERARD

in estrous, each observer was randomly assigned one female. If there were more estrous females than observers, the females to be followed were chosen at random. Behavioral data collection on the assigned focal females would begin between 08:00 to 09:00 and last until 18:00. Behavioral data were collected five days a week while data on estrous states were collected seven days a week.

All social, sexual, and aggressive behaviors with males were recorded on checksheets. All adult males and females within a 5-m radius of the focal female were recorded every fifth minute. The female's position in relation to the group was also recorded every fifth minute.

The social ranks of all males greater than 4 yr of age were determined from dyadic interactions prior to the onset of the mating season for each year of the study. Dominance interactions were recorded ad libitum (ALTMANN, 1974) throughout the mating season. For each year, a linear dominance hierarchy was constructed. Four-yr-old males were included because they are known to have sired offspring on Cayo Santiago (BERARD et al., 1994).

Two major categories of males were used for the analysis, long-term residents (LTR) and new males. LTRs were males in the group for four or more years, or the adult males present when the group fissioned in 1986. Males were classified as new if they were sexually mature and in the group for three years or less. For some analyses, new males were further subdivided into immigrant males and maturing natal males. Immigrant males were classified as new for their first three years in the social group. Maturing natal males were considered new from the ages of 4 to 6 (their first three years of mating in the group). Immigrant males and maturing natal males were then classified as LTRs their fourth breeding year in the group. Thus if a male immigrated into the group in 1988, he would be considered a new male through 1990. Beginning in 1991 (his fourth breeding season in the group) he would become a LTR. All three classes of males mated during the study and are known to have sired offspring (BERARD et al., 1993, 1994).

Two measures of reproductive activity were used. The number of ejaculations was used for data sets within each year of the study (e.g. correlations). To control for differences in the amount of data collected when comparing classes of males across years, the number of ejaculations was transformed to the percentage of ejaculations for each year. This figure was derived by transforming each male's ejaculation number into a percentage of the total number of ejaculations for each year of the study. These yearly percentages of ejaculation were then added and/or averaged over the years for the different classes of males. For some analyses, data are combined across years such that data in Year 1 represents the first year a male is a LTR, or the first year a male immigrates into the group, regardless of the year the data were collected.

For some analyses, ejaculations were restricted to those occurring during conception cycles (determined by counting back 166 days from parturition; SILK et al., 1993). The total amount of ejaculations throughout the breeding season for all female cycles (Total Cycles) were used in other analyses. The number of ejaculations during conception cycles ranged from 54 to 189 (Table 1) and total number of ejaculation per year ranged from 106 to 582. Results are based on a total of 445 ejaculations during conception cycles and 1389 total ejaculations over the four years of data collection. It should be noted that these data are not strictly independent. The data for some analyses were cross-sectional, while longitudinal in others. Thus, some males contributed to one year of data, while others contributed to multiple years.

STATISTICAL ANALYSIS

Only males who were group members were included in the analysis. Nonparametric tests were performed according to ZAR (1996). All tests were two-tailed and the significance level was set at p<0.05. Differences in ejaculation frequencies among the categories of males were


tested using a chi-square analysis. The expected values were calculated under the null hypothesis that the frequency of ejaculation was random among the male categories.

RESULTS

DOMINANCE RANK AND REPRODUCTIVE ACTIVITY

Correlations were made between male rank and number of ejaculations for each year of the study (Table 2). Significant positive correlations were derived in 1998 and 1990, and non- significant correlations in 1991 and 1992 for the total number of ejaculations. In restricting the analysis to ejaculations during conception cycles, there were significant correlations between rank and ejaculation frequency for one of the four years (1988), although correlations approached significance in 1991. Thus the association between male rank and reproductive activity, even within the same group, is not consistent over time.

To further explore the relationship between rank and reproductive activity, the hierarchy was divided into thirds (high, medium, and low) for each year. Table 3 provides the total number of ejaculations throughout the mating season and for ejaculations during conception cycles according to rank category. There was a significant difference in ejaculation number across the three rank categories in each year for all cycles (1988: ~2=63.94, df=2, p<0.001; 1990: Z2=42.2, df=2, p<0.001; 1991: ~2=219.1, df=2, p<0.001; 1992: ~2=205.4, df=2, p<0.001) and during conception cycles (1988: Z2=67.73, df=2, p<0.001; 1990: ~2=23.72, df=2, p<0.001 ; 1991 : Z2=55.16, df=2, p<0.001; 1992: ~2=42.24, df=2, p<0.001) .

High-ranking males had the greatest number of ejaculations and the only positive deviation from expected values the first two years of the study. They also had significantly more ejaculations than mid- and low-ranking categories combined for all cycles (1988: Z2=61.9, df=l, p<0.001; 1990: Z2=33.2, df=l, p<0.001) and conception cycles (1988: ~2=67.4, df=l,

Table 2. Spearman rank-order correlation coefficients for rank and ejaculation frequency by year for Total cycles and Conception cycles.

1988 (N= 13) 1990 (N= 17) 1991 (N=23) 1992 (N=22) Total cycles .605* .456* .275 .082 Conception cycles .604* .259 .411 .029

N: The number of males. *p<0.05.

Table 3. Observed and expected number of ejaculations over Total cycles and during Conception cycles for each year by male rank.

Rank 1988 1990 1991 1992 category Obs Exp N Obs Exp N Obs Exp N Obs Exp N

Total cycles

Conception cycles

High 70 32.6 4 126 83.6 6 232 202.4 8 115 147.6 7 Middle 26 40.8 5 69 69.7 5 305 177.1 7 310 168.7 8 Low 10 32.6 4 42 83.6 6 45 202.4 8 39 147.6 7

High 45 16.9 4 36 19.1 6 69 51.1 8 48 60.1 7 Middle 8 20.8 5 10 16.2 5 71 44.7 7 121 68.7 8 Low 2 16.9 4 8 19.1 6 7 51.1 8 20 60.1 7

Obs: Observed number of ejaculations; Exp: expected number of ejaculations; N: number of males in each rank category.

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p<0.001; 1990: )~2=23.13, df=l, p<0.001). High-ranking males had approximately the expected number of ejaculations in 1991, but fewer than expected ejaculations in 1992.

Mid-ranking males had fewer ejaculations than expected in 1988 and 1990. However, they had significantly more ejaculations than high plus low-ranking males in 1991 (all cycles: X 2= 132.8, df= 1, p<0.001; conception cycles: X2=33.1, dr= 1, p<0.001) and 1992 (all cycles: )~2=152.3, df=l, p<0.001; conception cycles: Z2=62.5, df=l, p<0.001) and the greatest positive deviations from expected values for these two years. Low-ranking males had the lowest number of ejaculations and negative deviations of ejaculations than expected in all four years.

Because the conclusions and interpretations from these data would differ if this had only been a one-year study, the data were analyzed as two 2-year "studies. In the first two years, high- ranking males had a combined 196 ejaculations, versus 96 for mid-ranking males and 52 for low-ranking males 0~2=95.6, df=2, p<0.001). High-ranking males accounting for 74.3% of ejaculations during conception cycles and had the only positive deviation from expected values (X2=83.3, df=2, p<0.001). Thus at the end of two years, with significant positive correlations each year, and a large advantage in ejaculation frequency during conception cycles, the only conclusion would have been that rank is the prime determinant of mating success in rhesus macaques.

Data over the latter two years of the study would have resulted in a dramatically different outcome. There was no significant correlation between rank and reproductive activity for either of the two years. Mid-ranking males did the majority of matings during conception cycles (ejaculation numbers: High = 117, Mid = 192, and Low = 27; )~2 = 121.9, df= 2, p<0.001) and over all cycles (High=347, Mid=615, and Low=84; X2=221.3, df=2, p<0.001). The conclusion would have been that rank had little effect on mating activity in rhesus macaques.

EJACULATION FREQUENCY AND TENURE

One proposed explanation for the differences in the association between rank and reproductive activity is the effect of residency time on mating frequency. Separate analyses of ejaculation frequencies over time were performed for males of three residency categories: long-term residents, recent immigrants, and natal males.

Long-term residents: Table 4 provides the mean percentage of ejaculations per male according to the number of years as a LTR. Data from the yearly mean number of ejaculations were combined and averaged according to the years as a LTR. Year 1 represents the first year a male is a long-term resident independent of the year the data were collected. Year 2 combines all of the second years for LTRs, and so on. For example, the mean percentage of a male who first became a LTR in 1988 was combined and averaged with the mean percentage of a male who became a LTR in 1991. The ejaculation frequency of the LTR males significantly decreases over time for total cycles (Kruskal-Wallis test statistic= 14.0, df=2, p=0.003) and conception cycles (Kruskal-Wallis test statistic=8.8, df=2, p=0.032). For ejaculation percentage over all cycles, there was no statistically significant difference from Year 1 to Year 2 (U lo,9=43.5, NS), but a significant decrease in ejaculation percentage from Year 2 to Year 3 (U 9,7=56.0, p=0.01). Although there is a decrease from Year 3 to Year 4, this difference was not significant (U 7,4=21.5, NS).

The percentage of ejaculation per male during conception cycles followed a similar pattern. The ejaculation percentage did not significantly differ from Year 1 to Year 2 (U 10,9=43.5, NS). Although there was a fourfold decrease in ejaculation percentage from Year 2 to Year 3, this

Dominance and Reproductive Activity in Rhesus Macaques

Table 4. Mean percentage of ejaculation per male for each year of residency for the immigrant, and natal.

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male categories, LTR,

Total cycles Conception cycles Number of males LTR Year 1 9.61 +4.10 10.25 +6.24 10

Year 2 9.92+3.25 11.84+5.88 9 Year 3 1.81 - 1.28 3.20+2.19 7 Year 4 0.85 +0.79 0.13 +0.13 4

Immigrants

Natal

Year 1 3.76_+1.13 2.84_+1.35 10 Year 2 8.36+2.41 6.71 +2.54 7 Year 3 9.38+2.14 10.15+3.85 4

Year 1 1.00+0.31 0.39+0.21 9 Year 2 3.27_ 1.28 3.10+ 1.58 10 Year 3 4.66+ 1.38 3.58+ 1.95 5 Year 4 6.81 + 1.93 6.31 +2.90 7 Year 5 8.90+2.88 6.88_+4.00 4 Year 6 0.73_+0.09 1.33_+0.46 3

Values are means+standard error. See text for definitions.

was not significant (U9,7=42.0, NS). The decrease from Year 3 to Year 4 was significant (U 7,4=27.5, p=0.009).

To further explore the relationship of decreasing reproductive activity of LTRs over time, comparisons were made for the same males who were LTRs in two consecutive years. The five males who were LTRs in both 1988 and 1990 showed a significant decrease in ejaculation frequency for all cycles (z = - 2 . 0 2 3 , p=0.043) , but not for conception cycles (z = - 1.483, NS). In comparing LTR males from 1990 and 1991 (N=5), a significant decrease was also found for all cycles ( z = - 2 . 0 2 3 , p=0.043) , but not during conception cycles ( z = - 0 . 6 7 7 , NS). In comparing the ejaculation frequency for six males who were LTR in 1991 and 1992, there was a significant decrease for both all cycles (z = - 2 . 2 0 7 , p=0.027) and conception cycles (z = -2 .226, p=0.026) . Thus, in comparing the same males from year-to-year, there were significant yearly decreases in ejaculation frequency for LTR in total cycles, and yearly decreases in conception cycles, although these decreases were significant only between 1991 and 1992.

Within the LTRs were four non-natal males who remained in the group over a four-year period during the duration of the study. These males occupied the first through third and fifth positions in the hierarchy and had been with the group since its inception in 1986. These four males exhibited a more dramatic decrease in mating success than the full sample of LTRs. Their yearly declines in percentage of ejaculations was from 16.1 to 9.7% to 2.6 to 0.89% in Year 4 (Friedman test statistic=7.5, df=3, p=0.007). The yearly decline in ejaculations during conception cycles approached significance (Friedman test statistic=7.5, df=3, p=0.058) . This pattern of a yearly decline in the percentage of total ejaculations and ejaculations during conception cycles was present for all four males; none of the four had an increase in any year.

Immigrants: Table 4 summarizes the data pooled from all the immigrant males. Data were derived in a similar manner as the LTR (see above) but year refers to year of immigration. The ejaculation rate per immigrant male started low their first year in the group (each male averaged just under 4% of the ejaculations) and then increased each subsequent year. The immigrant males had an overall threefold increase in ejaculation frequency from Year 1 to Year 3 (U 10,4=6.0, p=0.047). Although immigrant males increased their ejaculation frequency each year over their first three years in the group, the significant increase was between the second

166 J, BERARD

and third year (U 7,4 = 13.0, p=0.036). The number of ejaculations per immigrant male during conception cycles quadrupled from Year 1 to Year 3, but this increase was not significant. Each immigrant male averaged 10% of ejaculations during conception cycles his third year in the group. In contrast to LTR males, the mating pattern of immigrant males is one of increasing reproductive activity from year-to-year.

Maturing natal males: Most males disperse from their natal group at puberty although some remain through sexual maturity (KOFORD, 1963; CHAPAlS, 1983b; BERARD, 1990). A number of natal males became sexually mature during the study and mated in their natal group. These males ranged in age from 4 (N=9) to 9 (N=3) and occupied various rank positions. The amount of reproductive activity by natal males changed predictably with age (Table 4). Year refers to year of breeding, beginning with age 4. Thus year two equals age 5, year three equals age 6, etc. Ejaculation frequency increased every year through the age of 8, then decreased at nine years of age (Kruskal-Wallis test statistic= 15.49, df=5, p=0.008). The yearly increments in ejaculation frequency from age 4 through 8 were gradual and no year-to-year changes were significant. However, there was a significant increase in ejaculation frequency between the ages of 4 and 6 for all cycles (U9,5=6.5, p=0.032) as well as conception cycles (U9,5=8.5, p=0.046). The decrease in mating success between the ages of 8 and 9 was also significant (U4,3=12.0, p=0.034). The mating pattern of maturing natal males prior to emigration was a gradual increase in reproductive activity from ages 4 through 8, with a decrease at 9 yr of age.

The patterns of reproductive activity for males of all three classes show specific changes with time. The patterns that emerge are: (1) decreases in mating success for long-term resident males; (2) increases in mating success for recent immigrants; and (3) increases in mating success for maturing natal males. The number and tenure length of LTR males, the number and frequency of immigrants, and the number and age of maturing natal males will have a direct effect on correlations between rank and reproductive behavior and would have powerful implications for understanding the nature of the relationship between rank and reproduction.

YEARLY MATING PATTERNS

The reported variations in the correlation between rank and reproductive behavior may be explained by the life-history stages of the individual males in the social group. The changes in the number of males per category and their correspondent rates of ejaculation may account for some variation in the relationship between rank and reproductive activity. In the following section, the proportions of ejaculations of LTR males and new males will be compared for each year of the study. Table 5 provides the overall percentages of ejaculations for LTRs and new males over a four-year period.

In the first year of the study, the LTR males had a significantly greater percentage of ejaculations than new males during all cycles (1988: ~=49 .3 , df= 1, p<0.001) and conception cycles (1988: ~2=47.2, df= 1, p<0.001). LTR males also had significantly more ejaculations than the new males when the new category was divided into immigrant and natal males (total cycles: ~2=54.27, df=2, p<0.001; conception cycles: E2=49.59, df=2, p<0.001). Although both categories of new males had fewer ejaculations than expected, the degree of negative deviation from expected values for natal males was greater than that of immigrant males. A significant positive correlation between rank and reproductive activity was found in 1988.

Although there was a slight decrease in the percentage of ejaculation by LTR and an increase by new males in 1990, LTR males continued to have significantly more ejaculations than new


males (total cycles: )~2=35.92, df= 1, p<0.001; conception cycles: )~2=23.36, df= 1, p<0.001). Once again, immigrant males and natal males had fewer ejaculations than expected. However, unlike 1988, immigrant males had far fewer ejaculations than expected and natal males approached the expected value.

The pattern of a reproductive advantage to LTR males began to change in 1991. For the first time, LTR males had fewer than 50% of the ejaculations while new males had more than 50%, although this difference was not significant for either total cycles (X2=1.2, df=l, NS) or conception cycles ()~2=5.21, dr=l, NS). By 1991, the long-term residents had been with the group for at least five years and the recent immigrants for one or two years. When the categories of males were divided into LTRs, immigrants and natal males, the immigrant males had the highest percentage of ejaculations (total cycles: ~(2=72.37, df=2, p<0.001; conception cycles: )C 2= 11.28, df=2, p<0.005). This was also the first year a significant positive correlation between rank and reproductive activity was not found.

Table 5. Percentage of ejaculations for each year by LTR males and new males. Total cycles Conception cycles

Males 1988 1990 1991 1992 1988 1990 1991 1992 LTR 71.7 60.3 41.5 28.0 83.6 74.1 48.4 25.9

(5) (7) (9) (9)

New 28.3 39.7 58.7 71.9 16.4 25.9 51.9 74.0 (8) (10) (14) (13)

Immigrant 22.7 17.8 47.1 48.7 16.4 14.8 37.5 48.0 (4) (6) (8) (7)

Natal 5.6 21.9 11.6 23.2 0.0 11.1 14.4 26.0 (4) (4) (6) (6)

New males are also divided into immigrants and natal males. The number in parenthesis is the number of males in that category.

By the fourth year of the study, the new males had approximately 2.5 times the number of ejaculations than LTR males for both total cycles (Z 2 =31.88, df= 1, p<0.001) and conception cycles (~2=17.3, df=l, p<0.001). In 1992, immigrant males had the highest percentage of ejaculations of the three male categories (total cycles: Z2=63.19, df=2, p<0.001; conception cycles: Z2=26.37, df=2, p<0.001) and was the only category to have more ejaculations than expected.

In summary, LTR males had a greater than expected number of ejaculations in 1988 and 1990, the expected number in 1991, and had fewer than expected in 1992. Immigrant males had fewer than expected in 1988 and 1990, then greater than expected number of ejaculations and the highest percentages of ejaculations in 1991 and 1992. Natal males had fewer than expected ejaculations during all four years. The shift in the frequency of ejaculations from LTRs to new males mimicked the reported changes in the correlation values. Rank was clearly associated with ejaculation frequency in the first two years of the study, but not significantly associated with ejaculation frequency in 1991 and 1992 when mid-ranking males had the majority of ejaculations. These changes may reflect the great increase in ejaculation frequency for immigrant males their third year in the group and the great decrease in ejaculation frequency for LTR males their sixth year in the group.

168 J. BERARD

DISCUSSION

Understanding the nature of the relationship between male rank and reproductive behavior has been elusive. A number of longer-term studies on non-human primates have tbund that high-ranking males have a reproductive advantage in some years, but not in others (DuVALL et al., 1976; Wlrr et al., 1981; TAKAHATA, 1982; CUmE-COHEN et al., 1983; NISH1DA, 1983; STERN & SMITH, 1984; CHENEY et al., 1988; RUEHLMANN, 1989; HUFFMAN, 1991; SMITH, 1993, 1994; GUST et al., 1998). The length of the present study was a critical determinant in attempting to understand the dynamic nature of the rank/mating relationship. Depending on the year, the data would have clearly stated that rank was (1) unequivocally, (2) possibly, or (3) was not a major determinant of male reproductive activity. Extrapolating the evolutionary significance of rank on reproduction would have led to different explanations, based on the year of this study, or even over a two-year period. A major difficulty in extrapolating the results from one-year studies is that they provide no historical context in which to interpret the results. A significant or non-significant correlation from a short-term study reveals little about the processes involved in determining when high rank results in increased access to sexually receptive females. Because of this, results from any single year provide little information of the true relationship between rank and reproduction. Thus developing models based on single factor explanations deduced from short-term studies reveal little about the factors that truly influence reproductive activity and may mask evolutionary significant processes.

AGGRESSIVE COMPETITION, TENURE, DOMINANCE, AND REPRODUCTIVE ACTIVITY

Aggressive Competition in Rhesus Macaques

If either dominance or seniority were the primary determinant of reproductive success for male rhesus macaques, one could make two predictions. The first is that males should compete directly (e.g. aggressively) for rank. Although males may occasionally fight to improve their dominance position, or an individual male may immigrate into a group as an alpha male, rank is typically based on the tenure system (DRICKAMER & VESSEY, 1973; BERARD, 1990). Males tend to enter a group at the bottom of the hierarchy and passively increase positions in the hierarchy as higher-ranking animals die or emigrate and new animals immigrate into the group and occupy the bottom ranks. Thus rhesus macaques tend not to compete aggressively for rank. This ranking system has also been described in Japanese macaques (NORIKOSHI & KOYAMA, 1975; SPRAGUE et al., 1996; SPRAGUE, 1998).

The second prediction is that once males have achieved high rank, they should remain in the social group for as long as possible and not emigrate (VAN NOORDWIJK & VAN SCHAIK, 1985). However, high-ranking rhesus macaque males do emigrate from social groups (LINDBURG, 1969), in some years at the same rate as low-ranking males (BERARD, 1990). Massive emigration over a short period of time by a number of the highest-ranking males from a group has been observed on Cayo Santiago (pers. obs.). In addition, males that emigrate from groups do not receive more aggression prior to emigrating than males who remain (BERARD, 1990). Taken together, these results demonstrate that male-male competition alone is not sufficient to explain mating patterns. Because males are not aggressively competing for rank, high rank must not necessarily be the primary determinant for access to estrous females in rhesus macaques. Indeed, BERARD et al. (1993) and SMITH (1993, 1994) have demonstrated that low-ranking males have some degree of reproductive success.


Perhaps the most direct manner in which rhesus males aggressively compete for access to estrous females is through consort intrusion. However, males who disrupt consorts do not gain access to the female, nor are they successful in preventing the disrupted consort from resuming the mount sequence (WILSON, 1981; CHAPAIS, 1983a; HUFFMAN, 1987; MANSON, 1994a). In addition, males who disrupt consorts most frequently have the least degree of mating and reproductive success (BERARD et al., 1993). Thus consort intrusion, as a method of male-male competition over access to sexually-receptive females, is not a very successful reproductive tactic.

Immigration and Reproductive Activity

Two contrasting means of forming and maintaining male dominance hierarchies have evolved within the Cercopithecines that live in multi-male groups. In one system, dominance is inversely related to tenure, such that males join a group at high rank and decrease in rank with time (i.e. top entry). The second system is characterized by a direct relationship between rank and tenure. Males enter a group at low rank and increase their position in the hierarchy with increased tenure (i.e. bottom entry). In species where tenure length is directly tied to dominance rank, high-rank and tenure length are not independent attributes of males. The relationship between immigration, rank, aggressive competition, and reproductive activity will lie not so much in the dominance rank per se, but rather in the relative reproductive payoff to high rank.

Immigrant males should aggressively compete for high rank when rank directly translates into a significant reproductive advantage. The highest-ranking male baboons (ALTMANN et al., 1996) and crab-eating macaques (DE RUITER et al., 1992) have a significant reproductive advantage over their lower-ranking counterparts. In both of these species, immigrant males compete for the alpha position, join groups at a high rank and then decrease in rank over time (baboons: PACKER, 1979a.; STRUM, 1982; HAMILTON 8,: BULGER, 1990; NOE & SLUIJTER, 1990; crab-eating macaques: WHEATLEY, 1982; VAN NOORDWIJK & VAN SCHAIK, 1985, 1988; DE RUITER & VAN HOOFF, 1993; DE RUITER et al., 1994). Males that fail to compete for and attain high rank will most likely not reproduce (ALTMANN et al., 1996).

In species where immigrants enter at a low position (Japanese and rhesus macaques: see above for references) there is little aggressive competition for high rank. Moreover, high- ranking rhesus males (BERARD et al., 1993, 1994) and Japanese macaque males (INOUE et al., 1991, 1993; SOLTlS et al., 1997) do not necessarily have a reproductive advantage over their lower-ranking counterparts. For these species, there is no need to aggressively compete for high rank if the risk of aggression is greater than the reproductive payoff of high rank, or if low- ranking males can achieve some degree of mating and reproductive success without fighting. A rhesus macaque male that risks aggressively competing for and attaining high rank may not out- reproduce the lower-ranking males.

Despite the contrasting rank-order systems, both scenarios have two facets in common. Firstly, the newer males, regardless of the rank at which they join the group, tend to mate and reproduce. Male immigrants receive more solicitations from females in Japanese macaques (WOLFE, 1984; HUFFMAN, 1991), rhesus macaques (MANSON, 1995), and baboons (PACKER, 1979a, b). Tibetan macaque (M. thibetana) females mate with the new immigrants who tend to enter the group at high rank (ZHAO, 1994, 1996), a pattern previously described for baboons and crab-eating macaques. Even in species where bottom entry is common, males do occasionally enter a group at high rank and enjoy a high degree of reproductive activity (LINDBURG, 1983).

The second facet is that male reproductive activity is inversely proportional to tenure, regardless of the dominance system. For Japanese and rhesus macaques, some top-ranked males have little mating, or mate less than expected (STEPHENSON, 1975; ENOMOTO, 1978; TAKAHATA, 1982;

170 J. BERARD

CHAPA1S, 1983a; HILL, 1987; MCM1LLAN, 1989; PERLOE, 1992)whereas mid-ranking males may have more matings than high-ranking males (TAKAHATA, 1982; MCMILLAN, 1989; HUFFMAN, 1991). In species where there is a significant payoff to rank, increased tenure is associated with decreased mating opportunities (which is associated with decreased rank) (DE RUITER et al., 1992, 1994; BAUERS & HEARN, t994; ALTMANN et al., 1996). It may not be a general rule that rank is directly associated with a high degree of mating activity, but rather that new males increase their mating activity - independent of dominance rank - and it eventually decreases with increased tenure length.

The pattern of increased mating by immigrants and decreasing mating with increased tenure may simply be the reflections of patterns of mate selection and partner preferences over time. In rhesus and Japanese macaques, there is a cessation of sexual activity between pairs after the first two or more years of mating (TAKAHATA, 1982; HUFFMAN, 1992). On Cayo Santiago, only 17% of unique male-female dyads (121 of 690) mated in two consecutive years, 4.5% mated over three years and 0.5% for four years (BERARD, 1993). Although males with long tenure are sexually active and actively pursue mating opportunities, their decline in matings is attributed to female avoidance of their mating attempts (ENOMOTO, 1978; TAKAHATA, 1982; HUFFMAN, 1991, 1992; PERLOE, 1992). Indeed, it has been demonstrated that female mate choice and partner preference play an important role in macaque mating systems (HUFFMAN, 1991, 1992; MANSON, 1992) and that female choice can be the stronger predictor of male mating than male-male competition (SOLTIS et al., 1997). Females are avoiding mating with males who are familiar (PUSEY, 1980; MANSON • PERRY, 1993; MANSON, 1994b) and are preferring males that are novel mating partners (MANSON, 1995).

The tendency for estrous females to show interest in sexually unfamiliar males appears to be a widespread phenomenon (PACKER, 1979a, b; HENZl & LUCAS, 1980; SMUTS, 1985; HUFFMAN, 1992). Gorilla females tend to avoid mating with males who were dominant when the females were younger (STEWART & HARCOURT, 1987). Female chimpanzees avoid mating with old males from their natal group (PusEY, 1980) and chimpanzee males tend to prefer stranger females as mating partners (MORIN, 1993). Females moving to the group periphery to mate with non-resident, unfamiliar males has been reported in species with a multi-male structure (Japanese macaques: ENOMOTO, 1978; TAKAHATA, 1982; YAMAGIWA, 1985; SPRAGUE, 1991, 1992; rhesus macaques: LINDBURG, 1969, 1983; BERARD et al., 1994; vervets: HENZl & LAWES, 1987; blue monkeys: CORDS, 1984; CORDS et al., 1986), a one-male structure (langurs: LAWS & LAWS, 1984; patas: CHISM & ROWELL, 1986; CHISM & ROGERS, 1997), and in monogamous species (gibbons: REICHARD, 1995). Non-resident males have also sired offspring (OHSAWA et al., 1993; BERARD et al., 1994).

It is not a question of whether rank is or is not an important determinant of reproductive activity, but one of attempting to elucidate processes involved in making it important. Factors such as male age, tenure length, relationships with certain females, alternative strategies, and fighting ability interact when males compete for mating opportunities. Reproductive outcomes are not solely the result of male-male competition, but are also moderated by the relative contri- butions and interactions of female mate choice, female-female competition, and male mate selection (KuESTER & PAUL, 1996).

The observation that the influence of rank on reproductive behavior is variable over time within the same social group demonstrates that the rank/mating relationship is complex, certainly more complex than that predicted by the aggressive competition paradigm. It also support s the suggestion that the effect of rank on reproductive activity is not a predictable correlation, but rather a conditional probability (BERCOVlTCH, 1991). Both ex t r emes - that dominance alone determines reproductive activity or, alternately, that dominance is irrelevant - are


oversimplif ied assumptions about complex biological processes. Dominance does play an important role and its effect on mating patterns should not be underestimated. Dominance relationships provide useful estimates of an individual 's ability to compete (e.g. resource holding potential) and the mating strategy a male utilizes is dependent on his position in the hierarchy (HUFFMAN, 1992; BERARD et al., 1994). However, it is important to stress that dominance is not the only manner in which males compete; it is only one of many factors influencing the acquisition of limited resources. More detailed descriptions of how animals compete and how alternate strategies affect reproductive success may yield more rewarding insights regarding the relationship between rank and reproductive activity (STRUM, 1982, 1994; BERCOVlTCH, 1997; BERARD et al., 1994).

Acknowledgements. I would like to thank Drs. YUKIMARU SUGIYAMA, MIKE HUFFMAN, and JUICHI YAMAGIWA for the invitation to the symposium "Recent Trends in Primate Socioecology" in Inuyama, Japan. I especially thank MIKE WILLIAMS, LAURA MCGEEHAN, SOPHIA BALCOMB, COURTNEY SNYDER, and the 1988, 1990, 1991, and 1992 teams of interns for the data collection and Dr. MATT KESSLER for his support. Three anonymous reviewers provided useful comments on an earlier draft of this paper. Research was supported by NIH grant RR03640 to the Caribbean Primate Research Center, University of Puerto Rico Medical Sciences Campus and by the Committee to Integrate and Develop Scientific Research from the University of Puerto Rico Medical Sciences Campus.

REFERENCES

ALTMANN, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49: 227-267. ALTMANN, J.; ALBERTS, S. C.; HAINES, S. A.; DUBACH, J.; MURUTHI, P.; COOTE, T.; GEFFEN, E.; CHESSMAN,

D. J.; MUTUTUA, R. S.; SA1YALEL, S. N.; WAYNE, R. K.; LACY, R. C.; BRUFORD, M. W. 1996. Behavior predicts genetic structure in a wild primate group. Proc. Natl. Acad. Sci. USA, 93: 5797-5801.

ALTMANN, J.; HAUSFATER, G.; ALTMANN, S. A. 1988. Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Reproductive Success, CLUYFON-BROCK, T. H. (ed.), Univ. of Chicago Press, Chicago, pp. 403-418.

BAUERS, K. A.; HEARN, J. E 1994. Patterns of paternity in relation to male social rank in the stumptail macaque, Macaca arctoides. Behaviour, 129: 149-176.

BERARD, J. 1990. Life history patterns of male rhesus macaques on Cayo Santiago. Ph.D. thesis, Univ. of Oregon, Oregon.

BERARD, J. D. 1993. Male rank, mating success and dispersal: a four-year study of mating patterns in free- ranging rhesus macaques. Paper presented at the 16th Annual Meeting of the American Society of Primatologists, Sturbridge, Massachusetts.

BERARD, J. D.; NORNBERG, P.; EPPLEN, J. T.; SCHMIDTKE, J. 1993. Male rank, reproductive behavior, and reproductive success in free-ranging rhesus macaques. Primates, 34:481-489.

BERARD, J. D.; NORNBERG, P.; EPPLEN, J. T.; SCHMIDTKE, J. 1994. Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour, 129: 177-201.

BERCOVITCH, E B. 1986. Male rank and reproductive activity in savannah baboons. Int. J. Primatol., 7: 533 -550.

BERCOVITCH, E B. 1991. Social stratification, social strategies and reproductive success in primates. Ethol. Sociobiol., 12: 315-333.

BERCOVlTCH, E B. 1997. Reproductive strategies of rhesus macaques. Primates, 38: 247-263. BERENSTAIN, L.; WADE, T. D. 1983. Intrasexual selection and male mating strategies in baboons and

macaques. Int. J. Primatol., 4:201-235. BERNSTEIN, I. S. 1976. Dominance, aggression and reproduction in primate societies. J. Theor. Biol., 60:

459 -472. BERNSTEIN, I. S. 1981. Dominance: the baby and the bathwater. Behav. Brain Sci., 4: 419-457. CALDECOTT, J. O. 1986. Mating patterns, societies and the ecogeography of macaques. Anim. Behav., 34:

208 -220.

172 J. BERARD

CARPENTER, C. R. 1942. Sexual behavior of free ranging rhesus monkeys (Macaca mulatta). J. Comp. Physiol. Psychol., 33:113-142.

CHAPAIS, B. 1983a. Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav. Ecol. Sociobiol., 12: 215-228.

CHAPAIS, B. 1983b. Matriline membership and male rhesus reaching high ranks in their natal troops. In: Primate Social Relationships: An Integrated Approach, HINDE, R. A. (ed.), Sinauer, Sunderland, Massachusetts, pp. 171 - 175.

CHENEY, D. L.; SEYFARTH, R. M.; ANDELMAN, S J.; LEE, P. C. 1988. Reproductive success in vervet monkeys. In: Reproductive Success, CLUrrON-BRoCK, T. H. (ed.), Univ. of Chicago Press, Chicago, pp. 384-402.

CHISM, J.; ROGERS, W. 1997. Male competition, mating success and female choice in a seasonally breeding primate ( Erythrocebus patas ). Ethology, 103:109-126.

CHISM, J.; ROWELL, T. E. 1986. Mating and residence patterns in male patas monkeys. Ethology, 72:31-39. CONAWAu C. H.; KO~ORD, C. B. 1964. Estrous cycles and mating behavior in a free ranging band of rhesus

monkeys. J. Mammal., 45: 577-588. CORDS, M. 1984. Mating patterns and social structure in redtail monkeys (Cercopithecus ascanius). Z.

Tierpsychol., 64: 313-329. CORDS, M.; MITCHELL, B. J.; TSlNGALIA, H. M.; ROWELL, T. E. 1986. Promiscuous mating among blue

monkeys in the Kakamega forest, Kenya. Ethology, 72: 214-226. COWLISHAW, G.; DUNBAR, R. I. M. 1991. Dominance rank and mating success in male primates. Anim.

Behav., 41: 1045-1056. CURIE-COHEN, M.; YOSHIHARA, D.; LUTTRELL, L.; BENTORADO, K.; MACCLUER, J.; STONE, W. H. 1983. The

effects of dominance on mating behavior and paternity in a captive troop of rhesus monkeys (Macaca mulatta). Amer. J. Primatol., 5: 127-138.

DEWSBURY, D. A. 1982. Dominance rank, copulatory behavior and differential reproduction. Q. Rev. Biol., 57: 135-159.

DIXSON, A. E; BOSSl, T.; WICKINGS, E. J. 1993. Male dominance and genetically determined reproductive success in the mandrill (Mandrillus sphinx). Primates, 34: 525-532.

DRICKAMER, L. C. 1974. Social rank, observability, and sexual behavior of rhesus monkeys (Macaca mulatta). J. Reprod. Fertil., 37:117-120.

DRICKAMER, L. C.; VESSEY, S. H. 1973. Group changing in free ranging male rhesus monkeys. Primates, 14: 359-368.

DUVALL, S. W.; BERNSTEIN, I. S.; GORDON, T. P. 1976. Paternity and status in a rhesus monkey group. J. Reprod. Fertil., 47: 25-31.

ENOMOTO, T. 1978. On special preference in sexual behavior of Japanese monkeys (Macaca fuscata). J. Human Evol., 7: 283-293.

FA, J. E.; LINDBURG, D. G. (eds.). 1996. Evolution and Ecology of Macaque Societies. Cambridge Univ. Press, Cambridge.

FEDIGAN, L. M. 1983. Dominance and reproductive success. Yrbk. Phys. Anthropol., 26:91 -129. GUST, D. A.; McCASTER, T.; GORDON, T. P.; GERGITS, W. E; CASNA, N. J.; McCLURE, H. M. 1998.

Paternity in sooty mangabeys. Int. J. Primatol., 19: 83-95. HAMILTON, W. J.; BULGER, J. B. 1990. Natal male baboon rank rises and successful challenges to resident

alpha males. Behav. Ecol. Sociobiol., 26: 357-362. HENZI, S. E; LAWES, M. 1987. Breeding season influxes and the behavior of adult male samango monkeys

( Cercopithecus mitis albogularis). Folia Primatol., 48:125 - 136. HENZI, S. E; LUCAS, J. W. 1980. Observations on the inter-troop movement of adult vervet monkeys

(Cercopithecus aethiops). Folia Primatol., 33: 220-235. HILL, D. A. 1987. Social relationships between adult male and female rhesus macaques: I. Sexual consort-

ships. Primates, 28: 439-456. HUFFMAN, M. A. 1987. Consort intrusion and female mate choice in Japanese macaques (Macacafuscata).

Ethology, 75:221-234. HUFFMAN, M. A. 1991. Mate selection and partner preferences in female Japanese macaques. In: The

Monkeys ofArashiyama, FEDIGAN, L. M., ASQUITH, E J. (eds.), State Univ. of New York Press, Albany, New York, pp. 101-122.

HUFFMAN, M. A. 1992. Influences of female partner preference on potential reproductive outcome in Japanese macaques. Folia Primatol., 59: 77-88.

INOUE, M.; MITSUNAGA, F.; NOZAKI, M., OHSAWA, H.; TAKENAKA, A., SUGIYAMA, Y.; SHIMIZU, K., TAKENAKA, O. 1993. Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating. Primates, 34: 503-512.


INOUE, M.; MITSUNAGA, F.; OHSAWA, H.; TAKENAKA, A.; SUGIYAMA, Y.; GASPARD SOUMAH, A.; TAKENAKA, O. 1991. Male mating behavior and paternity discrimination by DNA fingerprinting in a Japanese macaque troop. Folia Primatol., 56: 202-210.

KAUFMANN, J. H. 1965. A three-year study of mating behavior in a free-ranging band of rhesus monkeys. Ecology, 46:500-512.

KOFORD, C. B. 1963. Rank of mothers and sons in bands of rhesus monkeys. Science, 141: 356-357. KUESTER, J.; PAUL, A. 1996. Female-female competition and male mate choice in Barbary macaques

(Macaca sylvanus). Behaviour, 133: 763-790. LAWS, J. W.; VONDER HAAR LAWS, J. 1984. Social interactions among adult male langurs (Presbytis

entellus) at Rajaji wildlife sanctuary. Int. J. Primatol., 5: 31-50. L1NDBURG, D. G. 1969. Rhesus monkeys: mating season mobility of adult males. Science, 166: 1176-1178. LINDBURG, O. G. 1983. Mating behavior and estrus in the Indian rhesus monkey. In: Perspectives in

Primate Biology, SETH, P. K. (ed.), Today & Tomorrow's Printers & Publ., New Delhi, pp. 45-61. LoY, J. 1971. Estrous behavior in free-ranging rhesus monkeys (Macaca mulatta). Primates, 12:1-31. MANSON, J. H. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques. Anim. Behav., 44:

405-416. MANSON, J. H. 1994a. Male aggression: a cost of female mate choice in Cayo Santiago macaques. Anim.

Behav., 48: 473-475. MANSON, J. H. 1994b. Mating patterns, mate choice, and birth season heterosexual relationships in free-

ranging rhesus macaques. Primates, 35: 417-433. MANSON, J. H. 1995. Do female rhesus macaques choose novel males? Amer. J. Primatol., 37: 285-296. MANSON, J. H.; PERRY, S. E. 1993. Inbreeding avoidance in rhesus macaques: whose choice? Amer. J.

Phys. Anthropol., 90: 285-288. MARRIOTT, B. M.; ROEMER, J.; SULTANA, C. 1989. An overview of the food intake patterns of the Cayo

Santiago rhesus monkeys (Macaea mulatta): report of a pilot study. Puerto Rico Hlth. Sci. J., 8: 87-94. MCMILLAN, C. A. 1989. Male age, dominance and mating success among rhesus macaques. Amer. J. Phys.

Anthropol., 80: 83-89. MOR1N, P. A. 1993. Reproductive strategies in chimpanzees. Yrbk. Phys. Anthropol., 36: 179-212. NISHIDA, T. 1983. Alpha status and agonistic alliance in wild chimpanzees (Pan troglodytes schwein-

furthii). Primates, 24: 318-336. NOE, R.; SLU1JTER, A. A. 1990. Reproductive strategies of male savannah baboons. Behaviour, 113:117-170. NORIKOSHI, K.; KOYAMA, N. 1975. Group shifting and social organization among Japanese monkeys. In:

Proceedings from the Symposia of the Fifth Congress of the International Primatological Society, KONDO, S.; KAWAI, M.; EHARA, A.; KAWAMURA, S. (eds.), Japan Science Press, Tokyo, pp. 43-61.

OHSAWA, H.; INOUE, M.; TAKENAKA, O. 1993. Mating strategy and reproductive success of male patas monkeys (Erythrocebus paras). Primates, 34: 533-544.

PACKER, C. 1979a. Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behav., 27:1-36. PACKER, C. 1979b. Male dominance and reproductive activity in Papio anubis. Anim. Behav., 27: 37-45. PAUL, A.; KUESTER, J.; TIMME, A.; ARNEMANN, J. 1993. The association between rank, mating effort, and

reproductive success in male Barbary macaques (Macaca sylvanus). Primates, 34:491-502. PERLOE, S. 1. 1992. Male mating competition, female choice and dominance in a free-ranging group of

Japanese macaques. Primates, 33: 289-304. PUSEY, A. 1980. Inbreeding avoidance in chimpanzees. Anim. Behav., 28: 543-552. RAWLINS, R. G.; KESSLER, M. J. (eds.). 1986. The history of the Cayo Santiago colony. In: The Cayo Santiago

Macaques: History, Behavior and Biology, State Univ. of New York Press, Albany, New York, pp. 13-46.

REICHARD, U. 1995. Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology, 100: 99-112. RUEHLMANN, T. E. 1989. Mate selection in rhesus macaques (Macaca mulatta). Ph.D. thesis, Univ. of

Georgia, Georgia. DE RUITER, J. R.; VAN HOOFF, J. A. R. A. M. 1993. Male dominance rank and reproductive success in

primate groups. Primates, 34: 513-524. DE RUITER, J. R.; VAN HOOFF, J. A. R. A. M.; SCHEFFRAHN, W. 1994. Social and genetic aspects of paternity

in wild long-tailed macaques. Behaviour, 129: 203-223. DE RUITER, J. R.; SCHEFFRAHN, W.; TROMMELEN, G. J. J. M.; UITERLINDEN, A. G.; MARTIN, R. D.; VAN

HooF, J. A. R. A. M. 1992. Male social rank and reproductive success in wild long-tailed macaques. In: Paternity in Primates: Genetic Tests and Theories, MARTIN, R. D.; DIXSON, A. F.; WICK1NGS, E. J. (eds.), Karger, Basel, pp. 175-191.

174 J. BERARD

SADE, D. S.; CHEPKO-SADE, B. D.; SCHNEIDER, J. M.; ROBERTS, S. S.; RICHTSME1ER, J. T. 1985. Basic Demographic Observations on Free-ranging Rhesus Monkeys. Human Relations Area Files, New Haven, Connecticut.

SINK, J.; SHORT, J.; ROBERTS, J.; KUSNITZ, J. 1993. Gestation length in rhesus macaques (Macaca mulatta). Int. J. Primatol., 14: 95-104.

SMITH, D. G. 1993. A 15-year study of the association between dominance rank and reproductive success of male rhesus macaques. Primates, 34:471-480.

SMITH, D. G. 1994. Male dominance and reproductive success in a captive group of rhesus macaques ( Macaca mulatta). Behaviour, 129: 225- 242.

SMUTS, B. B. 1985. Sex and Friendship in Baboons. Aldine, New York. SMUTS, B. B. 1987. Sexual competition and mate choice. In: Primate Societies, SMUTS, B. B.; CHENEu D. L.;

SEYFARTH, R. M.; WRANGHAM, R. W.; STRUHSAKER, T. T. (eds.), Chicago Univ. Press, Chicago, pp. 385-399.

SOLTIS, J.; MITSUNAGA, E; SHIMIZU, K.; NOZAK1, M.; YANAGIHARA, Y.; DOMINGO-ROURA, X.; TAKENAKA, O. 1997. Sexual selection in Japanese macaques, lI: Female mate choice and male-male competition. Anim. Behav., 54: 737-746.

SPRAGUE, D. S. 1991. Mating by nontroop males among the Japanese macaques of Yakushima Island. Folia Primatol., 57: 156-158.

SPRAGUE, D. S. 1992. Life history and male intertroop mobility among Japanese macaques (Macaca fuscata). Int. J. Primatol., 13: 437-454.

SPRAOUE, D. S. 1998. Age, dominance rank, natal status, and tenure among male macaques. Amer. J. Phys. Anthropol., 105: 511-521.

SPRAGUE, D. S.; SUZUKI, S.; TSUKAHARA, T. 1996. Variation in social mechanisms by which males attained the alpha rank among Japanese macaques. In: Evolution and Ecology of Macaque Societies, FA, J. E.; LINDBURG, D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 459-472.

STEPHENSON, G. R. 1975. Social structure of mating activity in Japanese macaques. In: Contemporary Primatology, KONDO, S.; KAWAI, M.; EHARA, A., KAWAMURA, S. (eds.), Japan Science Press, Tokyo, pp. 65-115.

STERN, B. R.; SMITH, D. G. 1984. Sexual behavior and paternity in three captive groups of rhesus monkeys (Macaca mulatta). Anim. Behav., 32: 23-32.

STEWART, K. J.; HARCOURT, A. H. 1987. Gorillas: variation in female relationships. In: Primate Societies, SMUTS, B. B.; CHENEY, D. L.; SEYFARTH, R. M.; WRANGHAM, R. W.; STRUHSAKER, T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 155-164.

STRUM, S. C. 1982. Agonistic dominance in male baboons: an alternative view. Int. J. Primatol., 3: 175-202. STRUM, S. C. 1994. Reconciling aggression and social manipulation as a means of competition: 1. Life-

history perspective. Int. J. Primatol., 15: 739-765. SUGIYAMA, Y. 1971. Characteristics of the social life of bonnet macaques (Macaca radiata). Primates, 12:

247- 266. TAKAHATA, Y. 1982. The socio-sexual behavior of Japanese monkeys. Z. Tierpsychol., 59: 89-108. TUTIN, C. E. G. 1979. Mating patterns and reproductive strategies in a community of wild chimpanzees.

Behav. Ecol. Sociobiol., 6: 29-38. VAN NOORDWIJK, M. A.; VAN SCHAIK, C. P. 1985. Male migration and rank acquisition in wild long-tailed

macaques (Macaca fascicularis). Anim. Behav., 33: 849-861. VAN NOORDWIJK, M. A.; VAN SCHAIK, C. P. 1988. Male careers in Sumatran long-tailed macaques (Macaca

fascicularis). Behaviour, 107: 24-43. WHEATLEY, B. P. 1982. Adult male replacement in Macacafascicularis of East Kalimantan, Indonesia. Int.

J. Primatol., 3: 203-219. WILSON, M. E. 1981. Social dominance and female reproductive behavior in rhesus monkeys (Macaca

mulatta). Anim. Behav., 29: 472-482. WITT, R.; SCHMIDT, G., SCHMIDT, J. 1981. Social rank and Darwinian fitness in a multimale group of

Barbary macaques (Macaca sylvanus L.). Folia Primatol., 36:201-211. WOLFE, L. D. 1984. Japanese macaque female sexual behavior: a comparison of Arashiyama East and

West. In: Female Primates: Studies by Female Primatologists, SMALL, M. E (ed.), Alan R. Liss, New York, pp. 141-158.

YAMAGIWA, J. 1985. Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates, 26: 105-120.


ZAR, J. H. 1996. Biostatistical Analysis. Prentence Hall, Upper Saddle River, New Jersey. ZHAO, Q.-K. 1994. Mating competition and intergroup transfer of males in Tibetan macaques (Macaca

thibetana) at Mt. Emei, China. Primates, 35: 57-68. ZHAO, Q.-K. 1996. Etho-ecology of Tibetan macaques at Mt. Emei, China. In: Evolution and Ecology of

Macaque Societies, FA, J. E.; LINDBUR6, D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 263-290.

- - Received: May 12, 1998; Accepted: October 26, 1998

Author's Name and Address: JOHN BERARD, Caribbean Primate Research Center, P. O. Box 906, Punta Santiago, Puerto Rico 00741, U.S.A. e-mail: [email protected]

Documents

A Four-year Study of the Association Between Male Dominance Rank, Residency Status, and Reproductive Activity in Rhesus Macaques (Macaca mulatta)